Publication: Bulletin of the World Health Organization; Type: Research
Article ID: BLT.13.130195
Chao Ma et al.
Progress towards measles elimination in China
This online first version has been peer-reviewed, accepted and edited,
but not formatted and finalized with corrections from authors and proofreaders.
Monitoring progress towards the elimination of measles in
China: an analysis of measles surveillance data
Chao Ma,a Lixin Hao,a Yan Zhang,b Qiru Su,a Lance Rodewald,c Zhijie An,a
Wenzhou Yu,a Jing Ma,a Ning Wen,a Huiling Wang,b Xiaofeng Liang,b
Huaqing Wang,a Weizhong Yang,b Li Lia & Huiming Luoa
a
National Immunization Programme, Chinese Center for Disease Control and Prevention, 27 Nanwei
Road, Xicheng District, Beijing, China.
b
Chinese Center for Disease Control and Prevention, Beijing, China.
c
World Health Organization, Beijing, China.
Correspondence to Huiming Luo (e-mail: hmluo@vip.sina.com).
(Submitted: 14 September 2013 – Revised version received: 28 December 2013 – Accepted: 31
December 2013 – Published online: 5 February 2014)
Abstract
Objective To analyse the epidemiology of measles in China and determine the
progress made towards the national elimination of the disease.
Methods We analysed measles surveillance data – on the age, sex, residence
and vaccination status of each case and the corresponding outcome, dates of onset
and report and laboratory results – collected between January 2005 and October 2013.
Findings Between 2005 and October 2013, 596 391 measles cases and 368
measles-related deaths were reported in China. Annual incidence, in cases per
100 000 population, decreased from 9.47 in 2008 to 0.46 in 2012 but then rose to more
than 1.96 in 2013. The number of provinces that reported an annual incidence of less
than one case per million population increased from one in 2009 to 15 in 2012 but fell
back to one in 2013. Median case age decreased from 83 months in 2005 to 14 months
in 2012 and 11 months in January to October 2013. Between 2008 and 2012, the
incidence of measles in all age groups, including those not targeted for vaccination,
decreased by at least 93.6%. However, resurgence started in late 2012 and continued
into 2013. Of the cases reported in January to October 2013, 40% were aged 8 months
to 6 years.
Conclusion Although there is evidence of progress towards the elimination of
measles from China, resurgence in 2013 indicated that many children were still not
being vaccinated on time. Routine immunization must be strengthened and the
remaining immunity gaps need to be identified and filled.
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Introduction
Measles is a highly infectious disease that causes enormous morbidity and mortality among
children in many parts of the world. For example, it has been estimated that measles and its
complications led to the deaths of more than 164 000 children in 20081 and about 139 300
children in 2010.2
The availability of safe and effective vaccines makes the global elimination of measles
possible, at least in theory. By 2011, the Region of the Americas of the World Health
Organization (WHO) had sustained measles elimination status for more than a decade. Four of
WHO’s other regions have adopted measles elimination targets, while the South-East Asia
Region has set itself the task of greatly reducing its measles-related mortality – to less than 5%
of the estimated value for the year 2000 – by 2015.3,4
In 2005, the Regional Committee for WHO’s Western Pacific Region resolved to
attempt to eliminate measles from the Western Pacific Region by 2012.5 In setting this target,
the Committee defined measles elimination as the absence of endemic measles transmission in
a defined geographical area for at least 12 months, in the presence of a well performing
surveillance system.6
China has a mainland population of more than 1.3 billion and an area of 9.6 million km2
and is the largest country in WHO’s Western Pacific Region. Despite substantial efforts to
eliminate measles from China in recent years, measles virus continues to circulate and cause
significant morbidity in the country and China accounts for a large proportion of the measles
cases reported in the Western Pacific Region.7,8 The elimination of measles in China is
therefore critical to achieving the goal of regional measles elimination.
In 1978, China established the national Expanded Programme on Immunization and
began to implement a standard schedule for routine immunization that included a dose of
measles vaccine administered at 8 months of age. A second routine dose of measles vaccine, at
7 years of age, was recommended in 1986. The 1997 national plan of action for accelerated
measles control called for measles vaccine coverage of at least 90%. The recommended age for
a child to receive a second dose of measles vaccine was lowered to between 18 and 24 months
in 2005.9 The mean annual measles incidence reported in China, in cases per 100 000
population, was 572.0 between 1960 and 1969, 355.3 between 1970 and 1979, 52.9 between
1980 and 1989, and 7.6 between 1990 and 1999,10 and it has remained below 10 since 2000.
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In 2006, China endorsed the 2006–2012 national action plan for measles elimination.
Subsequently, the country followed a comprehensive strategy for measles elimination, which
included immunization, measles surveillance and infection control. Estimated coverage with
the first dose of a vaccine containing measles virus increased from 80.4% in 2000 to 91.1% in
2009, while coverage with the second dose of such a vaccine increased from less than 80%
before 2005 to 84.3% in 2009.6 Between 2003 and 2009, 27 of the 31 mainland provinces of
China conducted unsynchronized province-wide supplementary immunization activities
against measles, with 185.7 million children targeted.6 In September 2010, China conducted
synchronized nationwide supplementary immunization activities against measles. These
nationwide activities, which ignored vaccination status, achieved a reported coverage of
97.52%.11
A national case-based system of measles surveillance with laboratory support has been
operational in China since 2009. Over the intervening years, the performance indicators for this
system have steadily improved.12 In 2011, the percentage of suspected measles cases
investigated within 48 hours of reporting (93.30%), the percentage of suspected measles cases
providing an adequate serum specimen (90.37%) and the percentage of serum specimens with
laboratory results reported within 7 days of specimen collection (93.85%) exceeded the
corresponding target values of 80% for each indicator.13
Programmes for the elimination of measles need to be monitored through the analysis of
surveillance data and performance indicators. We report an epidemiological description of data
collected in China’s national case-based system of measles surveillance since 2005, and discuss
the implications of our findings and the next steps needed for the elimination of measles from
China.
Methods
Although measles has been a notifiable disease in China since the 1950s, for many years only
aggregate data on measles incidence were submitted to the country’s national level. The
National Measles Surveillance Guidelines that were issued in 1998 recommended that
case-based measles surveillance be conducted in two selected provinces – Beijing and
Shanghai. When the Guidelines were updated, in 2003, it was recommended that such
surveillance should be expanded to cover 18 provinces. In 2005, China began to implement a
National Notifiable Disease Reporting System that permitted surveillance data to flow from
hospitals and county-level Centres for Disease Control to the national Centre for Disease
Control and Prevention, through a web-based computerized reporting system. The System
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Article ID: BLT.13.130195
collected information on the age, sex, location of residence, date of onset and occupation of
each suspected measles case.7,9 It was not until 2009 that the Ministry of Health asked that all of
China’s provinces conduct case-based measles surveillance. In this surveillance, a suspected
case of measles was defined as any person with fever and rash and one or more of the following
symptoms: cough, coryza and conjunctivitis. Also in 2009, the Ministry of Health asked that the
vaccination status and laboratory test results of each suspected measles case and the results of
any corresponding outbreak investigation be added to the information routinely collected by the
National Notifiable Disease Reporting System. In the routine examination of a suspected
measles case in China, a serum specimen is collected, sent to a measles laboratory and tested for
measles-specific IgM in a commercial enzyme-linked immunosorbent assay. Specimens for the
isolation of measles virus may also be collected and all of the resulting viral isolates are sent to
the National Measles Laboratory for genotyping.14
For this report, the case-based measles surveillance data reported to the national Centre
for Disease Control and Prevention between January 2005 and October 2013 were analysed. In
line with China’s current national measles surveillance guideline,15 which was updated in 2009
– i.e. before WHO determined that measles cases in the Western Pacific Region can no longer
be confirmed on clinical grounds alone – in this paper the term “measles case” refers to a case
confirmed by laboratory testing, epidemiological linkage or clinical criteria. These criteria
include (i) fever, (ii) a maculopapular rash and (iii) cough, coryza or conjunctivitis. Case
numbers were counted by date of onset and incidences – expressed as the number of cases per
100 000 or million population – were calculated using population denominators provided by
China’s National Bureau of Statistics.
Results
Between January 2005 and December 2012, 569 948 measles cases – including 344
measles-related deaths – were recorded in China. Overall, 59.9% of these cases were in males.
Annual numbers of cases over the same period ranged from 6183 in 2012 to 131 441 in 2008 –
representing annual incidences of 0.46 and 9.95 cases per 100 000 population, respectively.
Only 40.2% of the measles cases reported in this period were laboratory confirmed but the
percentage of cases that were laboratory confirmed increased from 28.7% in 2005 to 98.3% in
2012 (Fig. 1, Table 1).
Although 707 measles outbreaks were recorded between 2009 and 2012, the number,
size and duration of such outbreaks decreased annually over this period. The number of measles
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cases reported in the first 10 months of 2013 – 26 443 – was three times the number reported in
the whole of 2012 (Table 1).
Measles showed a similar seasonality in each year between 2005 and 2009, with peaks
in incidence in April and May and troughs in August through October (Fig. 1). The troughs in
incidence in 2010, 2011 and 2012 were relatively prolonged, from August to December. In
2012 there was no evidence of a peak in April and May, but incidence towards the end of the
year was relatively high (Fig. 1). The numbers of cases occurring in November 2012 (556) and
December 2012 (897) were 288% and 216% higher, respectively, than the corresponding
values in 2011. In 2013 there was, once again, a seasonal peak in April and May (Fig. 1).
Between 2005 and 2008, measles was endemic throughout the country. Over this
four-year period, no province had an annual incidence of less than one case per million
population and more than 86% of China’s counties reported at least one measles case each year.
Only one province (Ningxia) reported an annual incidence of at least 100 cases per million
population in 2009 but the number of such provinces rose to four (Beijing, Hebei, Heilongjiang
and Tianjin) in 2010 before falling back to one (Tibet) in 2011 and none in 2012. In contrast,
one province in 2009 (Hainan), three in 2010 (Fujian, Guangxi and Hainan), four in 2011
(Guangxi, Hainan, Jiangxi and Jilin) and 15 in 2012 reported measles incidences below one
case per million population. The percentage of China’s counties that reported at least one
measles case in the year decreased from 90.7% in 2008 to 36.4% in 2012. In the first 10 months
of 2013, no provinces reported a measles incidence of at least 100 cases per million population
but only one province (Heilongjiang) reported less than one measles case per million.
The mean and median ages of the measles cases reported between 2005 and 2012 were
125 and 52 months (interquartile range, IQR: 11–227), respectively. The median age of a case
decreased from 83 months (IQR: 13–227) in 2005 to 14 months (IQR: 8–252) in 2012 and just
11 months in January through October 2013. In each year that we investigated, the age group
showing the highest incidence of measles was either that of infants younger than 8 months –
that is, those who were too young to receive a first dose of measles-virus-containing vaccine –
or infants aged 8 to 23 months – that is, those who were eligible for one or both scheduled doses
of measles-virus-containing vaccine. The annual incidence of measles in each age group has
gradually decreased since 2008. Compared with the values for 2008, for example, the annual
incidences recorded in 2012 were 93.6%, 93.6%, 96.7%, 98.6%, 96.1% and 93.9% lower
among those aged less than 8 months, 8 to 23 months, 2 to 6 years, 7 to 14 years, 15 to 34 years
and more than 34 years, respectively. Between 2005 and 2012, the percentage of the year’s
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measles cases that occurred in infants aged less than 8 months increased from 11.3% to 24.5%
and the percentage of the year’s measles cases that occurred in children aged 8 to 23 months
increased from 19.4% to 33.9%. There were corresponding decreases in the percentages of the
year’s measles cases recorded among children aged 2 to 6 and 7 to 14 years, which fell from
21.4% to 11.9% and from 17.4% to just 2.4%, respectively. The percentage of the cases
reported in the first 10 months of 2013 that occurred in infants aged less than 8 months was
greater than the corresponding value for the whole of 2012 (31% versus 21%; Fig. 2).
The annual number of measles-related deaths ranged from 9 in 2012 to 103 in 2008
(Table 1). There were many more such deaths in the first 10 months of 2013 (n = 24) than in the
whole of 2012 (n = 9). Of the measles-related deaths that occurred in January through October
2013, 13 (54.2%), 8 (33.3%) and 3 (12.5%) were among children aged less than 8 months, 8 to
23 months and 24 to 82 months, respectively.
Of the 123 159 measles cases that were reported with residence information between
January 2009 and October 2013, only 9.4% had a record of migrating no more than 3 months
before they developed a rash but 47.8% were living in a county in which they had not been born
when their rash developed. The percentage of measles cases with known place of residence that
were living in a county in which they had not been born when their rash developed increased
steadily, from 36.8% in 2009 to 57.7% for the first 10 months of 2013. Paediatric cases of
measles were more likely to have vaccination records than the adult cases (Table 2). Overall,
31 159 cases aged 8 to 23 months were reported between January 2009 and December 2012.
Just over half (53%) of these cases were unvaccinated. The corresponding proportion for the
first 10 months of 2013 was relatively large (72%). Similarly, the proportion of cases aged 2 to
6 years that were unvaccinated was twice as high for the first 10 months of 2013 as for the
period from 2009 to 2012 (Table 2).
Between 2009 and 2012, genotype information was reported via the measles
surveillance system for just 1324 (1.2%) of the measles cases recorded over the same period. Of
the genotyped isolates, 1300 (98.2%) were genotype H1, one was D4, one was D8, one was
D11 and 15 were D9.
Genotype was also reported for more than 1600 (about 6.2%) of the measles cases
recorded in the first 10 months of 2013. Of the genotyped isolates made in 2013, 96% were H1,
2% were D9 and 2% were D8.
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Discussion
In 2006, China committed to eliminate measles and implemented strategies to interrupt the
indigenous transmission of measles virus. Our analysis of measles epidemiology from 2005 to
2012 showed a steady decrease in the annual incidence of measles in China. However, there
was a resurgence of measles in 2013, with a seasonal peak in April and May of that year. It
therefore appears that more effort will be needed to eliminate indigenous transmission of
measles virus in China.
The national incidence of measles in China decreased substantially – from 100 cases per
million population in 2008 to 4.6 cases per million in 2012 – before rebounding to 19.6 per
million in just the first 10 months of 2013. Similarly, although 15 of China’s 31 mainland
provinces reported annual incidences of measles below one case per million population in 2012,
only one province reported such a low incidence in the first 10 months of 2013. By 2011,
surveillance for measles in China at the national level was meeting most of WHO’s quality
criteria.16
Since 2008, most of the progress made in the elimination of measles in China has been
achieved through the concerted efforts of the national Expanded Programme on Immunization,
often in collaboration with the country’s educational system. The policies followed for measles
immunization in China have been similar to those used in countries that have successfully
eliminated measles. For example, China has implemented a two-dose policy of measles
vaccination for more than 25 years using effective measles vaccines. High coverages have been
achieved with both measles vaccine doses. Since 2009, for example, the first dose of
measles-virus-containing vaccine has reached more than 90% of the target population. China
also conducted province-level supplemental immunization activities with a measles vaccine
between 2003 and 2009. In 2010, it conducted a very large, nationwide campaign of
supplemental immunization activities against measles in which more than 100 million children
were vaccinated in a three-week period. China has also used checks on children entering
schools and kindergartens to help to ensure that school-age children are – or have been –
vaccinated against measles.
Before the implementation of the 2006 measles action plan – as well as in the action
plan’s early years – several of China’s provinces conducted supplemental immunization
activities that were designed to stop the transmission of measles virus among children aged
8 months to 14 years – that is, the age group with the highest incidence of measles. There were
two such provinces (Guizhou and Xinjiang) in 2004,17,18 two (Ningxia and Zhejiang) in 2005,19
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four (Hainan, Jilin, Qinghai and Tibet) in 2006 and three (Hebei, Shaanxi and four prefectures
of Sichuan) in 2007.20 In the years following these activities, dramatic decreases in the reported
incidence of measles cases were recorded in each of these provinces. However, these
province-level activities appeared to have little impact on measles incidence at the national
level. In 2008, for example, the national incidence of measles was higher than at any other time
in the past 15 years. Although a coordinated nationwide campaign of measles vaccination was
considered in 2008, such a campaign was prevented by limitations in the vaccine supply and
programme capacity and provinces were left to organize their own activities using a variety of
vaccination strategies.21 However, after a fairly large “catch-up” campaign of supplemental
immunization activities that covered 19 provinces in 2008 and 2009,22 there was a clear need
for a nationwide campaign. The 2010 nationwide campaign – again based on supplemental
immunization activities – seems to have been largely successful, since it was soon followed by
relatively low measles incidences. Encouragingly, the decreases seen in measles incidence
were not restricted to vaccine-targeted children but were also recorded among infants who were
too young to vaccinate and adults who were also not targeted in the campaign.
Additional efforts needed
The resurgence of measles in 2013 occurred primarily among young, unvaccinated children,
including infants who were too young to have been vaccinated and children of pre-school age
who had missed one or both of their scheduled vaccinations. Despite the use of strong policies
and programmes for measles vaccination, the H1 measles genotype continues to circulate in
almost all of China’s provinces. The H1 genotype is the only indigenous measles genotype in
China. Since there is no non-human reservoir for measles, the circulation of this genotype
represents person-to-person transmission that has persisted in China for at least 20 years.23
The elimination of measles in China will require all of the remaining immunity gaps to
be identified and filled – to the point that transmission of measles virus can no longer be
sustained. If immunity gaps are to be identified and adequately filled, case investigation and
outbreak analysis and response may all need to be improved. Measles virus is so highly
transmissible that it is able to travel along chains of transmission even among relatively well
vaccinated populations and infect groups of susceptible individuals – especially unvaccinated
young children.24 The resurgence of measles seen among young unvaccinated Chinese children
in 2013 indicates a weakness in routine immunization that allows some children to miss one or
both of their scheduled doses of measles vaccine. Such weakness must be eliminated if a further
resurgence in the next few years is to be avoided and measles is ever to be eliminated in China.
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The knowledge the routine programme of measles vaccination has weaknesses is
important. Surveillance and outbreak analysis can provide information about who is acquiring
measles and about the immunity gaps in target populations. Additional studies are needed to
identify why, in the routine programme, not all of the eligible children are being vaccinated in a
timely manner. Are children missing immunization opportunities at health-care encounters?
Are children who have recently relocated not being identified and enrolled in an immunization
clinic in a timely manner? Research on health services and health-care seeking may be useful in
identifying the reasons that some children are missing measles vaccinations. Such studies have
been found useful in countries that have already eliminated measles by strengthening routine
immunization25 and could well be beneficial in China.26 Records-based surveys of vaccine
coverage may also help to identify any gaps in population immunity and the main risk factors
for failure to be vaccinated.27
In China, huge numbers of individuals are currently migrating from rural areas to towns
and cities, largely in search of employment. Children who have moved county since birth –
including those of individuals who have relocated in this fashion – are less likely to be fully
vaccinated than local children.28–31 Improvements in the identification and location of children
who are new to an area may permit marked improvements in vaccine coverage.
In 2013, most of the resurgence seen in measles cases was the result of the susceptibility
of unvaccinated or incompletely vaccinated children – as has been the experience in some other
countries.32,33 In some of China’s provinces, however, 2013 saw an increasing incidence of
measles among adults. Although most adults in China are immune to measles, few have records
of their vaccination status. The resulting general inability to distinguish immune adults from the
non-immune without testing each individual makes campaigns of adult vaccination against
measles difficult or inefficient.
In conclusion, although substantial progress was made in China between 2005 and 2012
towards the elimination of measles, there was a resurgence of the disease – mostly among
young, unvaccinated children – in 2013. This resurgence started only two years after a
nationwide campaign based on supplementary immunization activities and occurred primarily
among children who became age-eligible for measles vaccination after that campaign. The
strengthening of routine immunization programmes, so that measles vaccine can be
administered on time to virtually all age-eligible children, is a challenge that will have to be met
in order for China to eliminate measles.
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Acknowledgements
We thank the staff of each province-, prefecture- and county-level Center for Disease Control
and Prevention. We are also grateful to Peter Strebel and Walter A Orenstein for their valuable
comments. Three of the authors (CM, LH and YZ) contributed equally to this article.
Competing interests:
None declared.
References
1. World Health Organization. Global reductions in measles mortality 2000–2008 and
the risk of measles resurgence. Wkly Epidemiol Rec. 2009;84:509-16.
PMID:19960624
2. Simons E, Ferrari M, Fricks J, Wannemuehler K, Anand A, Burton A et al.
Assessment of the 2010 global measles mortality reduction goal: results from a
model of surveillance data. Lancet. 2012;379:2173-8.
http://dx.doi.org/10.1016/S0140-6736(12)60522-4 PMID:22534001
3. World Health Organization. Progress in global control and regional elimination of
measles, 2000–2011. Wkly Epidemiol Rec. 2013;88:29-36. PMID:23393700
4. Measles elimination by 2020 [Internet]. New Delhi: World Health Organization
Regional Office for South-East Asia; 2013. Available from:
http://www.searo.who.int/mediacentre/releases/2013/pr1565/en/index.html
[cited 2014 Jan 9].
5. World Health Organization. Monitoring progress towards measles elimination. Wkly
Epidemiol Rec. 2010;85:490-4. PMID:21140596
6. Guidelines on verification of measles elimination in the Western Pacific Region.
Manila: World Health Organization, Western Pacific Region; 2013. Available
from:
http://www.wpro.who.int/immunization/documents/measles_elimination_verific
ation_guidelines_2013/en/index.html [cited 2014 Jan 9].
7. World Health Organization. Progress towards the 2012 measles elimination goal in
WHO’s Western Pacific Region, 1990–2008. Wkly Epidemiol Rec.
2009;84:271-9. PMID:19579325
8. Li J, Lu L, Pang X, Sun M, Ma R, Liu D, et al. A 60-year review on the changing
epidemiology of measles in capital Beijing, China, 1951–2011. BMC Public
Health. 2013;13:986. http://dx.doi.org/10.1186/1471-2458-13-986
PMID:24143899
9. Ma C, An Z, Hao L, Cairns KL, Zhang Y, Ma J, et al. Progress toward measles
elimination in the People’s Republic of China, 2000–2009. J Infect Dis.
2011;204 Suppl 1;S447-54. http://dx.doi.org/10.1093/infdis/jir103
PMID:21666198
10. Lixia W, Guang Z, Lee LA, Zhiwei Y, Jingjin Y, Jun Z, et al. Progress in accelerated
measles control in the People’s Republic of China, 1991–2000. J Infect Dis.
2003;187 Suppl 1;S252-7. http://dx.doi.org/10.1086/368045 PMID:12721922
Page 10 of 16
Publication: Bulletin of the World Health Organization; Type: Research
Article ID: BLT.13.130195
11. Ma C, Hao L, Ma J, Zhang Y, Cao L, Liang X, et al. Measles epidemiological
characteristics and progress of measles elimination in China, 2010. Chin J
Vaccin Immun. 2011;17:242-5. Chinese.
12. Ma C, Hao L, An Z, Ma J, Zhang Y, Xu W, et al. Establishment and performance of
measles surveillance system in the People’s Republic of China. Chin J Vaccin
Immun. 2010;16:297-306. Chinese.
13. Ma C, Su Q, Hao L, Zhang Y, Xu W, Luo H. Performance of measles surveillance
system in the People's Republic of China, 2011. Chin J Vaccin Immun.
2012;18:481-4. Chinese.
14. Xu W, Zhu Z, Jiang X, Zhang Y, Cui A, Mao N, et al. Establishment and running
status of measles laboratory network in China. Chin J Vaccin Immun.
2006;12:1-6. Chinese.
15. National Measles Surveillance Guideline. Beijing: Chinese Ministry of Health;
2009. Available from:
http://www.moh.gov.cn/jkj/s3581/200902/9ea8e400444c45b0a48e3e55d929c
9b5.shtml [cited 2014 Feb 2]. Chinese.
16. Measles elimination field guide [Internet]. Geneva: World Health Organization;
2013. Available from:
http://www.wpro.who.int/immunization/documents/measles_elimination_field_g
uide_2013.pdf [cited 2014 Jan 9].
17. Zuo S, Lian X, Yin D, You X, Guo B, Tong Y, et al. Measles Mass Campaign
experience and effect evaluation of Guizhou province, 2003-2004. Chin J
Vaccin Immun. 2006;12:7-12. Chinese.
18. Yu X, Liu Q, Guan J, Ma H, Re Y, Xu X, et al. Evaluation of measles mass
campaign of Xinjiang Uygur Automous Region in 2004. Chin J Vaccin Immun.
2006;12:373-5. Chinese.
19. Zhou L, Rui J, Fu Y, Li H, Li S, Lu W, et al. Evaluation measles mass campaign of
NingXia Hui Autonomous Region in 2005. Chin J Pest Control. 2007;23:820-2.
Chinese.
20. Ma C, Luo H, An Z, Zhang P, Wen N, Xia W, et al. Analysis on epidemiological
characteristics and measures of measles control in China during 2006-2007.
Chin J Vaccin Immun. 2008;14:208-13. Chinese.
21. Liang X, Yin D, Li L, Wang L, Zuo S, Wen N, et al. Requirement of measles vaccine
of the elimination of measles in China during period of 2006-2012. Chin J
Vaccin Immun. 2005;11:398-401. Chinese.
22.Hao L, Ma C, Ma J, An Z, Luo H, Liang X. Analysis on epidemiological
characteristics of measles in China from 2008-2009. Chin J Vaccin Immun.
2010;16:293-6. Chinese.
23. Zhang Y, Xu S, Wang H, Zhu Z, Ji Y, Liu C, et al. Single endemic genotype of
measles virus continuously circulating in China for at least 16 years. PLoS One.
2012;7:e34401. http://dx.doi.org/10.1371/journal.pone.0034401
PMID:22532829
24. Domínguez A, Torner N, Barrabeig I, Rovira A, Rius C, Cayla J, et al.; Working
Group for the Study of the Measles Outbreak in Catalonia. Large outbreak of
measles in a community with high vaccination coverage: implications for the
Page 11 of 16
Publication: Bulletin of the World Health Organization; Type: Research
Article ID: BLT.13.130195
vaccination schedule. Clin Infect Dis. 2008;47:1143-9.
http://dx.doi.org/10.1086/592258 PMID:18823269
25. Orenstein WA. The role of measles elimination in development of a national
immunization program. Pediatr Infect Dis J. 2006;25:1093-101.
http://dx.doi.org/10.1097/01.inf.0000246840.13477.28 PMID:17133153
26. Gao J, Chen E, Wang Z, Shen J, He H, Ma H, et al. Epidemic of measles following
the nationwide mass immunization campaign. BMC Infect Dis. 2013;13:139.
http://dx.doi.org/10.1186/1471-2334-13-139 PMID:23506461
27. Hinman AR, Orenstein WA, Papania MJ. Evolution of measles elimination
strategies in the United States. J Infect Dis. 2004;189 Suppl 1;S17-22.
http://dx.doi.org/10.1086/377694 PMID:15106084
28. Hu Y, Li Q, Luo S, Lou L, Qi X, Xie S. Timeliness vaccination of measles containing
vaccine and barriers to vaccination among migrant children in East China. PLoS
One. 2013;8:e73264. http://dx.doi.org/10.1371/journal.pone.0073264
PMID:24013709
29. Hu Y, Li Q, Chen E, Chen Y, Qi X. Determinants of childhood immunization uptake
among socio-economically disadvantaged migrants in East China. Int J Environ
Res Public Health. 2013;10:2845-56. http://dx.doi.org/10.3390/ijerph10072845
PMID:23839061
30. Hu X, Xiao S, Chen B, Sa Z. Gaps in the 2010 measles SIA coverage among
migrant children in Beijing: evidence from a parental survey. Vaccine.
2012;30:5721-5. http://dx.doi.org/10.1016/j.vaccine.2012.07.007
PMID:22819988
31. Sun M, Ma R, Zeng Y, Luo F, Zhang J, Hou W. Immunization status and risk factors
of migrant children in densely populated areas of Beijing, China. Vaccine.
2010;28:1264-74. http://dx.doi.org/10.1016/j.vaccine.2009.11.015
32. Muscat M, Bang H, Wohlfahrt J, Glismann S, Mølbak K; EUVAC.NET Group.
Measles in Europe: an epidemiological assessment. Lancet. 2009;373:383-9.
http://dx.doi.org/10.1016/S0140-6736(08)61849-8 PMID:19131097
33. Delaporte E, Wyler Lazarevic CA, Iten A, Sudre P. Large measles outbreak in
Geneva, Switzerland, January to August 2011: descriptive epidemiology and
demonstration of quarantine effectiveness. Euro Surveill. 2013;18:18.
PMID:23410259
Page 12 of 16
Publication: Bulletin of the World Health Organization; Type: Research
Article ID: BLT.13.130195
Table 1. Measles cases, January 2005–October 2013, China
Variable
Measles incidence (per 100 000 population)
No. of measles cases
Laboratory confirmation, % of cases
Male sex, % of cases
No. of measles-related deaths
Measles-related mortality, deaths per million
population)
No. of measles outbreaks reportedb
No. of measles cases in outbreaks
Median no. of cases per outbreak (range)
Median duration of outbreak, days (range)
2005
9.47
123 136
28.7
58
56
0.042
2006
7.62
99 602
29.8
59
35
0.027
2007
8.29
109 023
37.2
60
67
0.05
2008
9.95
131 441
39.9
60
103
0.077
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
Year
2009
3.95
52 461
56.2
61
37
0.029
2010
2.86
38 159
69.7
61
27
0.02
322
311
2205
1994
3 (2–203) 3 (2–88)
8 (1–114) 8 (1–163)
2011
0.74
9943
90.0
61
10
0.007
2012
0.46
6183
98.3
59
9
0.006
2013a
1.96
26 443
96.3
60
24
0.02
63
237
2 (2–15)
7 (1–56)
11
28
2 (2–5)
4 (1–13)
91
368
2 (2–29)
8 (1–44)
ND, no data.
a
The data shown for 2013 refer only to the first 10 months of the year.
b
In China, a measles outbreak is defined as the occurrence, within a 10-day period, of either at least two confirmed cases in a village, district, school or similar unit,
or at least five confirmed cases in a township.
Page 13 of 16
Publication: Bulletin of the World Health Organization; Type: Research
Article ID: BLT.13.130195
Table 2. Vaccination histories of measles cases, January 2009–October 2013, China
Month of onset
Jan 2009–Dec
2012
Jan–Oct 2013
Age group
< 8 months
8–23 months
2–6 years
7–14 years
≥ 15 years
All
< 8 months
8–23 months
2–6 years
7–14 years
≥ 15 years
All
No dose of
MCV
21 972 (100)
16 607 (53)
3931 (26)
1121 (17)
7398 (24)
47 673 (45)
8148 (100)
5629 (72)
1440 (53)
171 (28)
1436 (20)
16 555 (63)
Vaccination status, no. (%)
One dose of Two or more doses of
Unknown
MCV
MCV
0
0
0
7649 (25)
613 (2)
6290 (20)
3248 (21)
2998 (20)
4975 (33)
1093 (16)
1430 (21)
3148 (46)
1379 (4)
653 (2)
22 241 (70)
13 585 (13)
5706 (55)
39 782 (37)
0
0
0
1354 (17)
100 (1)
741 (10)
347 (13)
438 (16)
509 (18)
77 (13)
147 (24)
211 (35)
275 (4)
80 (1)
5340 (75)
2081 (8)
768 (3)
7039 (26)
Page 14 of 16
Total
21 972
31 159
15 152
6792
31 671
106 746
8148
7824
2734
606
7131
26 443
Publication: Bulletin of the World Health Organization; Type: Research
Article ID: BLT.13.130195
Fig. 1. Monthly numbers of measles cases, January 2005–October 2013, China
30 000
Confirmed by epidemiological linkage
Confirmed clinically
Confirmed by laboratory testing
20 000
s
e
s
ac
f
o
.
o
N
10 000
0
J M M J
2005
S N J
M M J
S
2006
N J M M J
2007
S N J M M J
2008
S N J M M J
S N J M M J
2009
2010
S N J M M J
S N J M M J
2011
Month of onset
MCV, measles-virus-containing vaccine.
a
The clinical criteria for case confirmation are (i) fever, (ii) a maculopapular rash and (iii) cough, coryza or conjunctivitis.
Page 15 of 16
2012
S N
J M M J
2013
S
Publication: Bulletin of the World Health Organization; Type: Research
Article ID: BLT.13.130195
Fig. 2. Yearly numbers of measles cases divided by age group, 2005–2013,
China
140 000
120 000
= 35 years
15–34 years
s 100 000
e
sa
c
f 80 000
o
.
o
N
60 000
7–14 years
2–6 years
8–23 months
< 8 months
40 000
20 000
0
2005 2006 2007 2008 2009 2010 2011 2012 2013
Year
Note: The data shown for 2013 refer only to the first 10 months of the year.
Page 16 of 16